Chemical Secretions of the Suborder Adephaga (Coleoptera)

Kelly B. Miller
Colorado State University
Fort Collins, Colorado 80523
The coleopteran suborder Adephaga contains eight families, all of which secrete a 
variety of glandular substances.а All families possess paired pygidial glands 
located postero-dorsally in the abdomen.а These glands open onto the eighth 
abdominal tergum.а Additionally, the families Dytiscidae and Hygrobiidae possess 
paired prothoracic glands.а The prothoracic glands of Dytiscidae secrete a variety 
of steroids, some of which are identical to typical vertebrate steroids, a 
phenomenon unique among Arthropoda.а The most widespread dytiscid steroid is 
deoxycorticosterone.а Pygidial glands are relatively uniform in structure throughout 
the suborder but vary in chemical constituents.а Dytiscidae, Gyrinidae and Carabidae 
are the families most studied.а Gyrinids produce unique norsesquiterpenes.а These 
are gyrinidal, isogyrinidal, gyrinidone and gyrinidione.а The most common pygidial 
gland compounds in Dytiscidae are aromatic aldehydes (e.g. p-hydroxybenzaldehyde), 
esters (e.g. methyl p-hydroxybenzoate) and acids (e.g. benzoic acid).а Dytiscids 
also produce many less widespread and/or more rare compounds.а Carabids also produce 
a diverse array of pygidial chemicals.а These are generally hydrocarbons, aliphatic 
ketones, saturated esters, formic acid, higher saturated acids, unsaturated 
aliphatic acids, phenols, aromatic aldehydes or quinones.а The most characteristic 
compounds are carboxylic acids, particularly formic acid, methacrylic acid and 
tiglic acid.а Among the more interesting compounds produced by carabids are 1,4 
quinones and hydroquinones ejected explosively by members of Brachinini. Other 
adephagan families are not as well known chemically.а All Adephaga deliver compounds 
in one of three ways depending on taxon.а These are
ааааааа 1) oozing,
ааааааа 2) spraying and
ааааааа 3) crepitation.
While many compounds have unknown functions, it is suspected that most compounds 
have one or more of six possible functions,
ааааааа 1) defense against vertebrate predators,
ааааааа 2) facilitation of penetration of defense compounds into predator integuments,
ааааааа 3) antimicrobial and antifungal (especially in Hydradephaga), 
ааааааа 4) increasing wetability of the integument (Hydradephaga), 
ааааааа 5) as alarm substances, 
ааааааа 6) as a propellant (Gyrinidae), and 
ааааааа 7) conditioning of plant tissues associated with oviposition.
Chemotaxonomy has been studied with Adephagan families with inconclusive results, 
mainly because of limited data.а Future research needs include identification of 
additional compounds, determination of function of compounds and application of this 
information to systematic, behavioral and ecological problems.
The suborder Adephaga represents a taxonomically well-defined group of beetles which 
exhibit a wide variety of chemical secretions and associated behaviors and 
ecological interactions.а Although a great deal of information on adephagan 
chemistry is available, no publications thoroughly address the entire suborder.а 
Apart from simply the interesting nature of the chemistry of these beetles, an 
understanding of the components of their glands could provide insight into 
relationships and evolutionary history of families within the group.а The taxonomy 
and systematics of adephagan families is not yet well resolved.
Review of families in Adephaga
Traditionally, the suborder has been divided into two groups.а The Hydradephaga is 
comprised of the Dytiscidae, Noteridae, Gyrinidae, Amphizoidae, Hygrobiidae and 
Haliplidae, all of which are aquatic.а The Geadephaga includes the terrestrial 
families Carabidae and Trachypachidae.аа Occasionally, Trachypachidae is treated as 
a subfamily of Carabidae, and Rhysodinae and Cicindelinae are often removed from 
Carabidae and given family status.а A great deal of evidence has shown Hydradephaga 
and Geadephaga to be probably artificial and not monophyletic (e.g. Beutel 1993; 
Beutel and Roughley 1988).а Adults of the great majority of members of these 
families are predaceous and/or, to a lesser degree, scavengers.а Exceptions include 
the mycophagous Rhysodinae (Carabidae), algophagous Haliplidae and some Noteridae, 
and some specialized phytophagous Carabidae.а Members of the suborder inhabit broad 
geographical and ecological distributions with some groups (most notably Carabidae 
and Dytiscidae) very speciose and often dominant members of systems in which they 
occur.а Other families, such as Trachypachidae or Amphizoidae, are much less 
influential ecologically since they contain only a few locally-occurring species.а 
However, they present interesting and valuable opportunities for study of beetle 
evolution and systematics.
Gland morphology
All Adephaga possess paired pygidial glands.а Forsyth (1970, 1972) provided some of 
the first and best descriptions of these structures in a comparative fashion, and he 
recognized several common features.а The pygidial glands exist as dorsally-located 
structures in the posterior end of the abdomen on each side of the hind gut and 
above the reproductive organs.а The glands open onto the eighth abdominal tergum and 
have no connection with the rectum.а They represent complex invaginations of the 
cuticle lined with epidermal cells contiguus with the integument.а The secretions 
pass from the gland secretory cell aggregations (secretory lobes) through a tube to 
a reservoir lined with muscles.а This reservoir narrows to a tube leading to an 
opening valve.а The secretory lobes may be elongate or oval and branched basally, 
apically or unbranched depending on taxon (Dettner 1985).а In some taxa, accessory 
glands may also be associated with the pygidial glands.а These open either intoа the 
reservoir or in the vicinity of the reservoir opening (Forsyth 1970, Dettner 1985). 
).а Gyrinids are unique in the extended shape of the external opening of the 
pygidial gland.а This may represent a specialized function of the gland substances 
as yet unknown (Scrimshaw and Kerfoot 1987).ааа In addition to the pygidial glands, 
the families Dytiscidae and Hygrobiidae (alone among Adephaga) possess paired 
prothoracic glands.а These are more simple in structure than the pygidial glands and 
consist only of reservoirs covered with secretory cells.а These open antero-
laterally on the prothorax near its margin in Dytiscidae and postero-laterally in 
Hygrobiidae (Dettner 1985).а In Dytiscidae, the glands are not lined with muscles 
and are relatively large while in Hygrobiidae they are smaller and lined with 
muscles (Dettner 1985).ааа In addition to these well known glands, many Adephaga 
possess other less-studied glands.а These include unicellular glands in the 
epidermis (Forsyth 1972) and glands in the foretarsi of males of some dytiscids 
which possibly secrete a "glue" or "sealant" for use during copulation (Aiken and 
Khan 1992).
Gland constituents
The variety of chemicals produced in the pygidial and prothoracic glands of Adephaga 
is extremely extensive.а Some compounds are relatively widespread among the suborder 
while others are unique to a specific group.
Gyrinids are unique in Adephaga in their production of norsesquiterpenes.а These 
compounds are gyrinidal, isogyrinidal, gyrinidone and gyrinidione.а Gyrinidal makes 
up about 50 percent of pygidial gland secretions and probably represents the 
precursor of the other three compounds (Oygur and Wolfe 1991).а Gyrinids are also 
known to make an aliphatic aldehyde and an alcohol (Dettner 1979).ааа Dytiscids are 
relatively well known chemically.а The prothoracic glands secrete a great variety of 
steroids.а Some of those isolated from Dytiscidae, such as estrone, estradial and 
testosterone (Scrimshaw and Kerfoot 1987) are characteristic steroids in 
vertebrates, a phenomenon unique in Arthropoda (Blum 1981).а Because of this, 
Dytiscids have been studied in greater detail than most of the other Hydradephaga.а 
Deoxycorticosterone is the most widespread prothoracic gland steroid in Dytiscidae 
(Gerhart et al. 1991).а Since insects cannot synthesize the precursors of the 
steroidal compounds they must be made from ingested cholesterol or related compounds 
derived from exogenous sources.а Fescemeyer and Mumma (1983) showed that ingested 
radioactivity labeled cholesterol was incorporated into the steroids of the 
prothoracic glands.а Alternatively, it is possible the precursors are produced by 
associated microorganisms (Swevers et al. 1991).а Other components of the dytiscid 
prothoracic glands include pregene and pregnediene derivatives and some alkaloids 
(Scrimshaw and Kerfoot 1987).ааа The pygidial glands secrete a large variety of 
compounds in dytiscids as well.а These are most commonly aromatic aldehydes, esters 
and acids (Scrimshaw and Kerfoot 1987).а The most common or widespread of these are 
p-hydroxybenzaldehyde, methyl p-hydroxybenzoate and benzoic acid (Blum 1981).а These 
compounds are frequently accompanied by several other compounds.а For example p-
hydroxybenzaldehyde is usually accompanied by p-hydroxybenzoic acid methyl ester 
(Scrimshaw and Kerfoot 1987).а Some groups also produce lactones, quinones, alpha 
hydroxycarbocyclic acids and forms of acetic or phenylpyruvic acids (Scrimshaw and 
Kerfoot 1987).
Members of Carabidae are also well studied in terms of pygidial gland constituents.а 
These generally fall into the following groups of compounds; hydrocarbons, aliphatic 
ketones, saturated esters, formic acid, higher saturated acids, unsaturated 
aliphatic acids, phenols, aromatic aldehydes and quinones (Moore 1977).а The most 
diverse type of compounds are the carboxylic acids, and the most widespread of these 
are formic acid, methacrylic acid and tiglic acid, although many others have been 
isolated (Blum 1981).а Individual species frequently produce a large number of types 
of carboxylic acids.а For example Davidson et al. (1989) isolated seven separate 
acids from Pasimachus subsulcatus.а Carabid chemical constituents can exhibit sexual 
dimorphism in some circumstances.а Attygalle et al. (1991) found tiglic acid to be 
absent in male Oodes americanus while it is present in the female.
а Other families of Adephaga are less well-known chemically, however, certain 
chemicals have been isolated.а Hygrobiids uniquely produce 2-hydroxyhexanoic acid 
and S-methyl-2-hydroxy-4-mercaptobutanoic acid (Dettner 1985).а Their prothoracic 
gland constituents are, as yet, unknown.а Noterids and some Hydroporinae 
(Dytiscidae) possess 3-indoleacetic acid which is a gall-producing plan hormone of 
unknown function in these beetles (Dettner 1985).а Benzoic acids and derivatives are 
present in Noteridae and Haliplidae (Dettner 1985).а No information has been 
published on chemicals present in Amphizoidae or Trachypachidae.
External delivery of compounds
Adephagan beetles deliver compounds in one of three ways; 1) oozing, 2) forceful 
spraying or 3) crepitation.а The glands of many groups are not equipped with muscles 
for discharging large amounts of substance (such as the prothoracic glands in 
Dytiscidae).а For this reason, these groups are only capable of more limited 
expulsion of compounds and the material oozes out from the openings.а This is in 
part facilitated by turgor pressure and by indirect action of nearby muscles 
(Scrimshaw and Kerfoot 1987).а In contrast, many groups, most notably Carabidae, 
have intrinsic muscles directly associated with the glands.а In this case, 
secretions can be ejected with varying amounts of force depending on taxon.а 
Pasimachus subsulcatus was found to be capable of forcibly discharging a spray of 
several centimeters (Davidson et al. 1989).а The final type of delivery, 
crepitation, is limited to the brachinine lineage of Carabidae and its near 
relatives.а This well known phenomenon has led them to be called bombardier beetles.а 
It is one of the more interesting delivery systems in Adephaga.а In these beetles, 
hydroquinones are stored together with hydrogen peroxide in the major gland 
chambers. .а The most commonly-occurring quinones are hydroquinones, 1,4-
benzoquinone and 2-methyl-1,4-benzoquinone (Blum 1981). аааCatalases and peroxidases 
are stored in an accessory chamber.а When the beetle is disturbed, these compounds 
are mixed.а This produces a strongly exothermic reaction which is easily detectable 
audibly as a "pop".а The quinones generated by this reaction are discharged as a 
vapor of about 100o C (Aneshansley et al. 1969).а The beetles frequently possess 
morphological adaptations such as elytral flanges used to direct the spray (Eisner 
et al. 1989).а Dean et al. (1990) showed that the emission occurs as a pulsed jet 
rather than as a steady stream.а They argue that this allows for a higher discharge 
velocity due to increased pressure in the reaction chamber.
Functions of glandular compounds
Although the functions of many compounds have not been extensively studied, ideas 
have been proposed for the possible function or functions of the various prothoracic 
and pygidial constituents produced by Adephaga.а Many compounds have been implicated 
as toxins or feeding deterrents against predators.а The huge amounts of steroids 
found in dytiscid prothoracic glands are undoubtedly associated with protection 
against vertebrates (Swevers et al. 1991).а Dytiscids are potentially subject to 
predation by fish, amphibians, birds and, possibly, small mammals.а Treatment of 
food pellets with pregn-4-en-20 alpha-ol-3-one and deoxycorticosterone significantly 
altered rates of acceptance of the pellets by Lepomis macrochirus (bluegill sunfish) 
in a study by Gerhart et al. (1991). The explosive emissions of brachinine carabids 
are very hot, an effective deterrent against predators.а Davidson et al. (1989) 
noted that the discharge of the carabid Pasimachus subsulcatus was irritating to the 
eyes and induced pain on abraded skin.а Gyrinids have been studied extensively for 
effects of their pygidial gland compounds on vertebrates.а The compounds have been 
shown to deter feeding in fish and newts by Benfield (1972) and Meinwald et al. 
(1972) or as defensive toxins against fish in high doses (Muller et al. 1975).а 
Morgan (1992) suggested that the bright, spotted coloration and aggregating behavior 
in Thermonectes marmoratus may be an example of aposematic coloration.ааа If some 
compounds do not directly deter predation in an of themselves, they may, 
alternatively, facilitate penetration of other compounds into predator integuments.а 
This possibility was suggested by Moore (1979) for the hydrocarbon, aliphatic ketone 
and saturated ester compounds of the pygidial glands of many carabids.а Since these 
chemicals are not generally toxins or deterrents, he suggested that they could 
disrupt waxy layers on a predator epicuticle making it easier for other irritating 
chemicals to penetrate.
Another possible direct defensive capability of many adephagan compounds is as 
antimicrobial or antifungal agents, particularly in Hydradephaga.а For example, 
marginalin may have some antimicrobial abilities by fixing spermin and spermidin on 
the cuticle or by interfering with carotenoids in invading cells thereby disrupting 
photosynthesis (Barbier 1990).а Dettner (1985) argued that pygidial chemicals are 
used primarily for their antimicrobial activity.а Compounds such as benzoic acid or 
phylacetic acid are well known for their antimicrobial and preservative 
capabilities.а Aquatic beetles can frequently be observed rubbing their legs over 
their bodies, presumably smearing secretions onto their surfaces (Dettner 1985).а 
Another supporting line of evidence is the observation that pygidial gland 
secretions in aquatic families are administered by oozing because of the lack of 
strong muscles for spraying of compounds.а Therefore, the compounds are emitted in 
relatively small amounts which may be more useful in antimicrobial activities than 
in large-predator deterrence.
Many compounds, including marginalin, are useful for increasing wetability (Barbier 
1990), a possible function experimentally supported by Dettner (1985).а This 
property would be useful for aquatic beetles that must leave the water and dry their 
cuticle in order to disperse.а The "cleaning" action of beetles when newly entering 
a body of water seems to indicate that this may be a function of their pygidial 
compounds (Dettner 1985).
аааа Henrikson and Stenson (1993) suggested that pygidial gland secretions may serve 
as alarm pheromones in Gyrinidae.а These beetles frequently aggregate in large 
numbers where communicating alarm could prove useful.а Blum (1981) suggested the 
same possibility for prothoracic steroids in Dytiscidae.а The fact that many species 
of Gyrinidae are often present in aggregations could indicate interspecific alarm 
communication in these species.а The sexual dimorphism of chemicals exhibited by 
some carabids (Attygalle et al. 1991) suggests their possible role as pheromones.
аааа Vulinec (1987) suggested that gyrinid pygidial gland secretions could serve, in 
part, as a propellant on water surfaces by lowering the surface tension.а However, 
this is probably only a secondary function to the well-supported predator-deterrence 
аааа A final possibility for some pygidial-gland chemicals is the conditioning of 
plant tissues where oviposition takes place.а 3-indoleacetic acid and phenyl acetic 
acid, which have been isolated from members of Noteridae and some Hydroporinae 
(Dytiscidae), are gall-producing plant auxins present in other insects who use it 
during endophytic oviposition (Dettner 1985).а However, this type of oviposition and 
associated gall-production has not been observed in these groups (Dettner 1985).
аааа In summary, the variety of chemicals produced by adephagan beetles may fulfill 
one or more of the following functions; 1) as invertebrate or vertebrate predator 
feeding deterrents or toxins, 2) to facilitate penetration of defense compounds into 
predator cuticle, 3) as antimicrobial or antifungal agents (Hydradephaga), 4) to 
increase wetability of the integument (Hydradephaga), 5) as alarm or other 
pheromones, 6) as swimming propellants (Gyrinidae), and 7) as conditioners of plant 
tissues for endophytic oviposition.
Chemotaxonomy and evolution of Adephagan chemicals
аааа Despite the potential for use in phylogenetic studies of the group, adephagan 
chemicals and gland morphology have been used relatively rarely in analyses of 
evolutionary relationships.аа A few studies, however, have used the nature of the 
chemicals in systematic studies.а Dettner (1979, 1985) developed a phylogeny of 
Hydradephaga based on pygidial gland constituents.а In this analysis Gyrinidae and 
Hygrobiidae occupied isolated positions.а However, Beutel (1986) placed Hygrobiidae 
as the sister-group of Dytiscidae based, in part, on the common presence of 
prothoracic defense glands in the two groups.а Dettner (1985) questioned the 
homology of these glands because of their very different morphologies.а If steroid 
compounds are found in hygrobiid prothoracic glands it could firmly establish the 
evolutionary relatedness of Hygrobiidae and Dytiscidae proposed by Beutel (1986) and 
others.а Moore (1979) suggested that chemical components of Carabidae could be 
valuable for carabid evolutionary studies.а It seems clear, however, that more data 
on adephagan chemistry is required before any far-reaching implications can be drawn 
regarding evolutionary relationships in the group.а Several groups are very poorly 
known chemically, and for some, such as Amphizoidae and Trachypachidae, nothing is 
known of their chemical compounds.
аааа Blum (1981) suggested that the prothoracic steroids produced by dytiscids may 
have been the reason for their relative evolutionary success.а Since all members of 
Adephaga possess pygidial glands and Adephaga is a relatively ancient lineage, 
perhaps the presence of chemical defenses has played some part in the success of the 
group as a whole.а Swevers et al. (1991) suggested that the "vertebrate type" of 
steroid hormone system may be a plesiomorphic character in Animalia based on the 
common presence of steroids in vertebrates and Dytiscidae.а However, it seems 
abundantly clear that the presence of "vertebrate" steroids in Dytiscidae represents 
convergence given the absence ofа these compounds in all other arthropods and the 
relatively derived nature of the family Dytiscidae within Adephaga (e.g. Beutel 
аааа Forsyth (1972) suggested evolution of the adephagan pygidial gland from a 
unicellular dermal gland.а An invagination of the cuticle would facilitate 
development of a reservoir for storage of compounds of utility.а Further 
modifications on this theme may have led to the variety in shapes of structures 
associated with adephagan glands.
аааа Adephagans are fantastic producers of chemicals in a variety of forms.а These 
chemical characters are, for the most part, clearly understudied in many groups and 
underused in phylogenetic, behavioral and ecological studies.а Several groups, such 
as Trachypachidae and Rhysodinae and Cicindelinae (Carabidae) have posed unresolved 
problems as to their correct phylogenetic placement.а A knowledge of the chemistry 
of these groups could shed light on their relationships.а In addition, much work 
remains to be done on the functional significance of many compounds, particularly in 
the area of possible pheromone activities.а Apparent aposematic coloration in some 
groups of Dytiscidae and Haliplidae could provide examples for studies of the 
evolution of this phenomenon.
Aiken, R. B. and A. Khan.а 1992.а The adhesive strength of the palettes of males of 
a boreal water beetle, Dytiscus alaskanus J. Balfour Browne (Coleoptera: 
Dytiscidae). Can. J. Zool.а 70:1321-1324. 
Aneshansley, D. J., T. Eisner, J. M. Widom and B. Widom.а 1969.а Biochemistry at 
100o C explosive secretory discharge of bombardier beetles (Brachinus).а Science 
Attygalle, A. B., J. Meinwald, T. K. Liebherr, and T. Eisner.а 1991.а Sexual 
dimorphism in theа defensive secretion of a carabid beetle.а Experimentia 47:296-
Barbier, M.а 1990.а Marginalin, a substance from the pygidial glands of Dytiscus 
marginalis (Coleoptera).а Molecular associations with polyamines in vitro.а 2.а 
Naturforch.а 45b:1455- 1456. 
Benfield, E. F.а 1972.а A defensive secretion of Dineutes discolor (Coleoptera: 
Gyrinidae).а Ann. Ent. Soc. Am.а 65:1324-1327. 
Beutel, R. G.а 1986.а Skelet und muskulatur des kopfes und thorax vou Hygrobia tarda 
(Herbst). Ein beitrag zur klarung der phylogenetischen benziehungen der Hydradephaga 
(Insectaаааааа Coleoptera). Stuttgarten Beitr. Naturk. (A) 388:1-54. 
Beutel, R. G.а 1993.а Phylogenetic anlysis of Adephaga (Coleoptera) based on 
characters of the larval head.а Systematic Ent.а 18:127-147. 
Beutel, R. G. and R. E. Roughley.а 1988.а On the systematic position of the family 
Gyrinidae (Coleoptera: Adephaga). Z. zool. Syst. Evolut.-forsch. 26:380-400. 
Blum, M. S.а 1981.а Chemical defenses of arthropods.а Academic Press. New York. 562 
Davidson, B. S., T. Eisner, B. Witz and J. Meinwald.а 1989.а Defensive secretion of 
the carabid beetle Pasimachus subsulcatus. J. Chem. Ecol. 15:1689-1697. 
Dean, J., D. J. Aneshansley, H. E. Edgerton, and T. Eisner.а 1990.а Defensive spray 
of the bombardier beetle: a biological pulse jet.а Science.а 248:1219-1221. 
Dettner, K.а 1979.а Chemotaxonomy of water beetles based on their pygidial gland 
constituents.Biochemical Systematics and Ecology.а 7:129-140. 
Dettner, K.а 1985.а Ecological and phylogenetic significance of defensive compounds 
from pygidial glands of Hydradephaga (Coleoptera). Proc. Acad. Nat. Sci. Phila. 
Eisner, T., G. E. Ball, B. Roach, D. Aneshansley, M. Eisner, C. Blankespoor and J. 
Meinwald. 1989.а Chemical defense of an Ozaenine bombardier beetle from New Guinea.а 
Psyche. 96:153-160. 
Fescemeyer, H. W. and R. O. Mumma.а 1983.а Regeneration and biosynthesis of dytiscid 
defensive agents (Coleoptera: Dytiscidae). J. Chem. Ecol. 9:1449-1463. 
Forsyth, D. J.а 1970.а The structure of the defence glands of the Cicindelidae, 
Amphizoidae and Hygrobiidae (Insecta: Coleoptera). J. Zool., Lond. 160:51-69. 
Forsyth, D. J.а 1972.а The structure of the pygidial defence glands of Carabidae 
(Coleoptera). Trans. Zool. Soc. Lond. 32:249-309. 
Gerhart, D. J., M. E. Bondura and J. A. Commito.а 1991.а Inhibition of sunfish 
feeding by defensive steroids from aquatic beetles:а structure-activity 
relationships.а J. Chem. Ecol. 17:1363-1370. 
Henrikson, B. T. and J. A. E. Stenson.а 1993.а Alarm substance in Gyrinus aeratus 
(Coleoptera, Gyrinidae).а Oecologia.а 93:191-194. 
Meinwald, J., K. Opheim and T. Eisner.а 1972.а Gyrinidal: a sesquiterpenoid aldehyde 
from the defense glands of gyrinid beetles. Proc. Nat. Acad. Sci. U.S.A. 69:1208-
Miller, J., L. B. Hendry and R. O. Mumma.а 1975.а Norsesquiterpenes as defensive 
toxins of whirligig beetles (Coleoptera: Gyrinidae).а J. Chem. Ecol.а 1:59-82. 
Morgan, R. C. 1992. аSunburst diving beetles: living jewels brighten rippling 
waters. Backyard Bugwatching. 14:4-10. 
Moore, B. P.а 1979.а Chemical defense in carabids and its bearing on phylogeny.а In 
T. L. Erwin, G. E. Ball, D. R. Whitehead, eds.а Carabid beetles: their evolution, 
natural history andа classification. Junk Publishers, The Hague. 
Oygur, S. and G. W. Wolfe.а 1991.а Classification, distribution and phylogeny of 
North American (north of Mexico) species of Gyrinus Muller (Coleoptera: Gyrinidae).а 
Bull. Am. Mus. Nat. Hist. 207:1-97. 
Scrimshaw, S. and W. C. Kerfoot.а 1987.а Chemical defenses of freshwater organisms: 
beetles and bugs. In W. C. Kerfoot and A. Sih, eds. Predation: direct and indirect 
impacts on aquatic communities.а Univ. Press. New England.а 386 pp. 
Swevers, L., J. G. D. Lambert and A. DeLoof.а 1991.а Synthesis and metabolism of 
vertebrate-type steroids by tissues of insects, a critical evaluation.а 
Experimentia.а 47:687-698. 
Vulinec, K.а 1987.а Swimming in whirligig beetles (Coleoptera: Gyrinidae) a possible 
role of the pygidial gland secretion.а Coleop. Bull.а 41:151-153.ааааааааааааааааааааааааааааа 


Сайт управляется системой uCoz